Effects of two selected resistance exercises and recreational sport activities on microRNA-148a expression and cardiometabolic risk factors of children with type 1 diabetes

Mohammed Kareem, Yasir; Minasian, Vazgen; Hovsepian, Silva; Nazari, Maryam

doi:10.22059/sshr.2024.380968.1155

Effects of two selected resistance exercises and recreational sport activities on microRNA-148a expression and cardiometabolic risk factors of children with type 1 diabetes

Document Type : Research Paper

Authors

¹ Department of Exercise Physiology, Faculty of Sport Sciences, University of Isfahan, Isfahan, Iran

² Metabolic Liver Disease Research Center, Isfahan university of medical sciences, Isfahan, Iran

³ Department of Exercise Physiology, Faculty of Sport Sciences, University of Isfahan, Isfahan

10.22059/sshr.2024.380968.1155

Abstract

Background: Metabolic diseases such as type 1 diabetes is considered the most important threat factor for cardiovascular complaint. Although the pathological mechanisms underpinning the development of T1D are delicate to define, better understanding of the molecular aspects is most important to identify new remedial targets.
Aim: Evaluating of the effect of two selected resistance and recreational sport activities on microRNA-148a expression and some biomarkers in children with type 1 diabetes.
Materials and Methods: Twenty type 1 diabetic children were assigned randomly to resistance exercise (RE), (n=10, age=12.6 years), and recreational sport activities (RSA), (n=10, age=12.4 years) groups. Participants engaged in an 8-week exercise training, 3 sessions/week. The miR-148-a, HbA1c, glucose, insulin, and HOMA-IR levels have been assessed before and after exercise interventions.
Results: Following the exercise interventions, the concentration of miR-148-a exhibited a non-significant increase in both groups. Nevertheless, no significant differences were noted in the reduction of insulin resistance or in the levels of insulin itself (P≤ 0.05). The level of HbA1c decreased but the cardio-respiratory endurance of subjects increased.
Conclusion: Both the resistance and recreational sport activities were effective to improve in cardiorespiratory fitness, diabetic markers, and miR-148a changes that seem to be indicative of the pathological status of type 1 diabetic children.

Keywords

References

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[11] King KM, Jaggers JR, Della LJ, McKay T, Watson S, Kozerski AE, et al. "Association between physical activity and sport participation on hemoglobin A1c among children and adolescents with type 1 diabetes". Int J Environ Res Public Health. 2021; 18(14): 7490. DOI: 10.3390/metabo12111017.

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[15] Femminò S, Pagliaro P. "Exercise prevents cardiovascular dysfunctions in diabetes through miRNAs modulation". Non-coding RNA Investig. 2021; 5: 1. DOI: 10.21037/ncri-20-8.

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[19] Liu S, Wu W, Tang F, Shen M, Xu W, Zhao S. "MicroRNA-21: A critical pathogenic factor of diabetic nephropathy". Front. Endocrinol. 2022: 1330. DOI: 10.3389/fendo.2022.895010.

[20] Margaritis K, Margioula-Siarkou G, Giza S, Kotanidou EP, Tsinopoulou VR, Christoforidis A, et al. "Micro-RNA implications in type-1 diabetes mellitus: A review of literature". Int. J. Mol. Sci. 2021; 22(22): 12165. DOI: 10.3390/ijms222212165.

[21] Shi C, Zhang M, Tong M, Yang L, Pang L, Chen L, et al. "miR-148a is associated with obesity and modulates adipocyte differentiation of mesenchymal stem cells through Wnt signaling". Sci. Rep. 2015; 5(1): 9930. DOI: 10.1038/srep09930.

[22] Nascimento LRd, Domingueti CP. "MicroRNAs: new biomarkers and promising therapeutic targets for diabetic kidney disease". Braz. J. Nephrol. 2019; 41: 412-22. DOI: 10.1590/2175-8239-JBN-2018-0165.

[23] Matsuzaka A, Takahashi Y, Yamazoe M, Kumakura N, Ikeda A, Wilk B, et al. "Validity of the multistage 20-m shuttle-run test for Japanese children, adolescents, and adults". Pediatr. Exerc. Sci. 2004; 16(2): 113-25. DOI: 10.1123/pes.16.2.113.

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[25] Tan Y, Lu X, Cheng Z, Pan G, Liu S, Apiziaji P, et al. "miR-148a regulates the stem cell-like side populations distribution by affecting the expression of ACVR1 in esophageal squamous cell carcinoma". Onco Targets Ther. 2020: 8079-94. DOI: 10.2147/OTT.S248925.

[26] Yuan K, Lian Z, Sun B, Clayton MM, Ng IO, Feitelson MA. "Role of miR-148a in hepatitis B associated hepatocellular carcinoma". PloS one. 2012; 7(4): e35331. DOI: 10.1371/journal.pone.0035331.

[27] Chen J, Bai X, Wu Q, Chen L, Wang H, Zhang J. "Exercise protects against cognitive injury and inflammation in alzheimer’s disease through elevating miR-148a-3p. Neurosci. 2023; 513: 126-33. DOI: 10.1016/j.neuroscience.2023.01.008.

[28] Li Y, Deng X, Zeng X, Peng X. "The role of Mir-148a in cancer". J. Cancer. 2016; 7(10): 1233. DOI: 10.7150/jca.14616.

[29] Nielsen S, Åkerström T, Rinnov A, Yfanti C, Scheele C, Pedersen BK, et al. "The miRNA plasma signature in response to acute aerobic exercise and endurance training". PloS one. 2014; 9(2): e87308. DOI: 10.1371/journal.pone.0087308.

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[31] Jin X, Hao Z, Zhao M, Shen J, Ke N, Song Y, et al. "MicroRNA-148a regulates the proliferation and differentiation of ovine preadipocytes by targeting PTEN". Animals (Basel). 2021; 11(3): 820. DOI: 10.3390/ani11030820.

[32] Li B, Feng F, Jia H, Jiang Q, Cao S, Wei L, et al. "Rhamnetin decelerates the elimination and enhances the antitumor effect of the molecular-targeting agent sorafenib in hepatocellular carcinoma cells via the miR-148a/PXR axis". Food Funct. 2021; 12(6): 2404-17. DOI: 10.1039/d0fo02270e.

[33] Melnik BC, Weiskirchen R, Schmitz G. "Milk exosomal microRNAs: friend or foe?—a narrative review". ExRNA. 2022; 4: 22. DOI: 10.21037/exrna-22-5.

[34] Robinson K, Baker L, Graham-Brown M, Ashford R, Pawluczyk I, Major R, et al. "Decreased miRNA-148a-3p expression in skeletal muscle of patients with chronic kidney disease". bioRxiv. 2022: 05.24.4931 94. DOI: 10.1101/2022.05.24.493194.

[35] Shi C, Zhu L, Chen X, Gu N, Chen L. "IL-6 and TNF-α induced obesity-related inflammatory response through transcriptional regulation of miR-146b". J Interferon Cytokine Res. 2014; 34. DOI: 10.1089/jir.2013.0078.

[36] Assmann TS, Recamonde-Mendoza M, de Souza BM, Crispim D. "MicroRNA expression profiles and type 1 diabetes mellitus: systematic review and bioinformatic analysis". Endocr Connect. 2017; 6(8): 773-90. DOI: 10.3390/children9081174.

[37] Calcaterra V, Magenes VC, Vandoni M, Berardo C, Marin L, Bianchi A, et al. "Benefits of Physical exercise as approach to prevention and reversion of non-alcoholic fatty liver disease in children and adolescents with obesity". Children. 2022; 9(8): 1174. DOI: 10.1530/EC-17-0248.

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Effects of two selected resistance exercises and recreational sport activities on microRNA-148a expression and cardiometabolic risk factors of children with type 1 diabetes

References

[1] Aljawarneh YM, Wardell DW, Wood GL, Rozmus CL. "A systematic review of physical activity and exercise on physiological and biochemical outcomes in children and adolescents with type 1 diabetes". J. Nurs. Scholarsh. 2019; 51(3): 337-45. DOI: 10.1111/jnu.12472.

[2] Ogle GD, von Oettingen JE, Middlehurst AC, Hanas R, Orchard TJ. "Levels of type 1 diabetes care in children and adolescents for countries at varying resource levels". Pediatr Diabetes. 2019; 20(1): 93-8. DOI: 10.1111/pedi.12801.

[6] Lu X, Zhao C. "Exercise and type 1 diabetes". Adv Exp Med Biol. 2020: 107-21. DOI: 10.1007/978-981-15-1792-1_7.

[7] Moser O, Eckstein ML, West DJ, Goswami N, Sourij H, Hofmann P. "Type 1 diabetes and physical exercise: moving (forward) as an adjuvant therapy". Curr. Pharm. Des. 2020; 26(9): 946-57. DOI: 10.2174/1381612826666200108113002.

[8] Chetty T, Shetty V, Fournier PA, Adolfsson P, Jones TW, Davis EA. "Exercise management for young people with type 1 diabetes: A structured approach to the exercise consultation". Front. Endocrinol. 2019; 10: 326.

[9] Farhan R, Alzubaidi M, Ghayyib S. "Fatty liver disease in children and adolescents with type 1 diabetes mellitus (clinical and diagnostic aspects)". J Clin Gastroenterol Hepatol. 2018; 2(2): 14. DOI: 10.21767/2575-7733.1000043.

[10] Khandelwal R, Dassanayake AS, Conjeevaram HS, Singh SP. "Non-alcoholic fatty liver disease in diabetes: When to refer to the hepatologist?". World J. Diabetes. 2021; 12(9): 1479. DOI: 10.4239/wjd.v12.i9.1479.

[11] King KM, Jaggers JR, Della LJ, McKay T, Watson S, Kozerski AE, et al. "Association between physical activity and sport participation on hemoglobin A1c among children and adolescents with type 1 diabetes". Int J Environ Res Public Health. 2021; 18(14): 7490. DOI: 10.3390/metabo12111017.

[12] Grabia M, Markiewicz-Żukowska R, Socha K, Polkowska A, Zasim A, Boruch K, et al. "Prevalence of metabolic syndrome in relation to cardiovascular biomarkers and dietary factors among adolescents with type 1 diabetes mellitus". Nutr. 2022; 14(12). DOI: 10.3390/nu14122435.

[13] de Gonzalo-Calvo D, Dávalos A, Montero A, García-González Á, Tyshkovska I, González-Medina A, et al. "Circulating inflammatory miRNA signature in response to different doses of aerobic exercise". J. Appl. Physiol. 2015; 119(2): 124-34. DOI: 10.1152/japplphysiol.00077.2015.

[14] Fernández-Sanjurjo M, de Gonzalo-Calvo D, Fernández-García B, Díez-Robles S, Martínez-Canal Á, Olmedillas H, et al. "Circulating microRNA as emerging biomarkers of exercise". Exerc Sport Sci Rev. 2018; 46(3): 160-71. DOI: 10.1249/JES.0000000000000148.

[15] Femminò S, Pagliaro P. "Exercise prevents cardiovascular dysfunctions in diabetes through miRNAs modulation". Non-coding RNA Investig. 2021; 5: 1. DOI: 10.21037/ncri-20-8.

[16] Grieco GE, Dotta F. The Essential Role of MicroRNAs in Diabetes Mellitus: Regulators of β Cell Function And Potential Disease Biomarkers. Ph.D thesis. 2020.

[17] Friedrich M, Pracht K, Mashreghi MF, Jäck HM, Radbruch A, Seliger B. "The role of the miR‐148/‐152 family in physiology and disease". Eur. J. Immunol. 2017; 47(12): 2026-38. DOI: 10.1002/eji.201747132.

[18] Improta Caria AC, Nonaka CKV, Pereira CS, Soares MBP, Macambira SG, Souza BSdF. "Exercise training-induced changes in microRNAs: beneficial regulatory effects in hypertension, type 2 diabetes, and obesity". Int. J. Mol. Sci. 2018; 19(11): 3608. DOI: 10.3390/ijms19113608.

[19] Liu S, Wu W, Tang F, Shen M, Xu W, Zhao S. "MicroRNA-21: A critical pathogenic factor of diabetic nephropathy". Front. Endocrinol. 2022: 1330. DOI: 10.3389/fendo.2022.895010.

[20] Margaritis K, Margioula-Siarkou G, Giza S, Kotanidou EP, Tsinopoulou VR, Christoforidis A, et al. "Micro-RNA implications in type-1 diabetes mellitus: A review of literature". Int. J. Mol. Sci. 2021; 22(22): 12165. DOI: 10.3390/ijms222212165.

[21] Shi C, Zhang M, Tong M, Yang L, Pang L, Chen L, et al. "miR-148a is associated with obesity and modulates adipocyte differentiation of mesenchymal stem cells through Wnt signaling". Sci. Rep. 2015; 5(1): 9930. DOI: 10.1038/srep09930.

[22] Nascimento LRd, Domingueti CP. "MicroRNAs: new biomarkers and promising therapeutic targets for diabetic kidney disease". Braz. J. Nephrol. 2019; 41: 412-22. DOI: 10.1590/2175-8239-JBN-2018-0165.

[23] Matsuzaka A, Takahashi Y, Yamazoe M, Kumakura N, Ikeda A, Wilk B, et al. "Validity of the multistage 20-m shuttle-run test for Japanese children, adolescents, and adults". Pediatr. Exerc. Sci. 2004; 16(2): 113-25. DOI: 10.1123/pes.16.2.113.

[25] Tan Y, Lu X, Cheng Z, Pan G, Liu S, Apiziaji P, et al. "miR-148a regulates the stem cell-like side populations distribution by affecting the expression of ACVR1 in esophageal squamous cell carcinoma". Onco Targets Ther. 2020: 8079-94. DOI: 10.2147/OTT.S248925.

[26] Yuan K, Lian Z, Sun B, Clayton MM, Ng IO, Feitelson MA. "Role of miR-148a in hepatitis B associated hepatocellular carcinoma". PloS one. 2012; 7(4): e35331. DOI: 10.1371/journal.pone.0035331.

[27] Chen J, Bai X, Wu Q, Chen L, Wang H, Zhang J. "Exercise protects against cognitive injury and inflammation in alzheimer’s disease through elevating miR-148a-3p. Neurosci. 2023; 513: 126-33. DOI: 10.1016/j.neuroscience.2023.01.008.

[28] Li Y, Deng X, Zeng X, Peng X. "The role of Mir-148a in cancer". J. Cancer. 2016; 7(10): 1233. DOI: 10.7150/jca.14616.

[29] Nielsen S, Åkerström T, Rinnov A, Yfanti C, Scheele C, Pedersen BK, et al. "The miRNA plasma signature in response to acute aerobic exercise and endurance training". PloS one. 2014; 9(2): e87308. DOI: 10.1371/journal.pone.0087308.

[30] Vasu S, Kumano K, Darden CM, Rahman I, Lawrence MC, Naziruddin B. "MicroRNA signatures as future biomarkers for diagnosis of diabetes states". Cell. 2019; 8(12): 1533. DOI: 10.3390/cells8121533.

[31] Jin X, Hao Z, Zhao M, Shen J, Ke N, Song Y, et al. "MicroRNA-148a regulates the proliferation and differentiation of ovine preadipocytes by targeting PTEN". Animals (Basel). 2021; 11(3): 820. DOI: 10.3390/ani11030820.

[32] Li B, Feng F, Jia H, Jiang Q, Cao S, Wei L, et al. "Rhamnetin decelerates the elimination and enhances the antitumor effect of the molecular-targeting agent sorafenib in hepatocellular carcinoma cells via the miR-148a/PXR axis". Food Funct. 2021; 12(6): 2404-17. DOI: 10.1039/d0fo02270e.

[33] Melnik BC, Weiskirchen R, Schmitz G. "Milk exosomal microRNAs: friend or foe?—a narrative review". ExRNA. 2022; 4: 22. DOI: 10.21037/exrna-22-5.

[34] Robinson K, Baker L, Graham-Brown M, Ashford R, Pawluczyk I, Major R, et al. "Decreased miRNA-148a-3p expression in skeletal muscle of patients with chronic kidney disease". bioRxiv. 2022: 05.24.4931 94. DOI: 10.1101/2022.05.24.493194.

[35] Shi C, Zhu L, Chen X, Gu N, Chen L. "IL-6 and TNF-α induced obesity-related inflammatory response through transcriptional regulation of miR-146b". J Interferon Cytokine Res. 2014; 34. DOI: 10.1089/jir.2013.0078.

[36] Assmann TS, Recamonde-Mendoza M, de Souza BM, Crispim D. "MicroRNA expression profiles and type 1 diabetes mellitus: systematic review and bioinformatic analysis". Endocr Connect. 2017; 6(8): 773-90. DOI: 10.3390/children9081174.

[37] Calcaterra V, Magenes VC, Vandoni M, Berardo C, Marin L, Bianchi A, et al. "Benefits of Physical exercise as approach to prevention and reversion of non-alcoholic fatty liver disease in children and adolescents with obesity". Children. 2022; 9(8): 1174. DOI: 10.1530/EC-17-0248.

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Effects of two selected resistance exercises and recreational sport activities on microRNA-148a expression and cardiometabolic risk factors of children with type 1 diabetes

References

[1] Aljawarneh YM, Wardell DW, Wood GL, Rozmus CL. "A systematic review of physical activity and exercise on physiological and biochemical outcomes in children and adolescents with type 1 diabetes". J. Nurs. Scholarsh. 2019; 51(3): 337-45. DOI: 10.1111/jnu.12472.

[2] Ogle GD, von Oettingen JE, Middlehurst AC, Hanas R, Orchard TJ. "Levels of type 1 diabetes care in children and adolescents for countries at varying resource levels". Pediatr Diabetes. 2019; 20(1): 93-8. DOI: 10.1111/pedi.12801.

[6] Lu X, Zhao C. "Exercise and type 1 diabetes". Adv Exp Med Biol. 2020: 107-21. DOI: 10.1007/978-981-15-1792-1_7.

[7] Moser O, Eckstein ML, West DJ, Goswami N, Sourij H, Hofmann P. "Type 1 diabetes and physical exercise: moving (forward) as an adjuvant therapy". Curr. Pharm. Des. 2020; 26(9): 946-57. DOI: 10.2174/1381612826666200108113002.

[8] Chetty T, Shetty V, Fournier PA, Adolfsson P, Jones TW, Davis EA. "Exercise management for young people with type 1 diabetes: A structured approach to the exercise consultation". Front. Endocrinol. 2019; 10: 326.

[9] Farhan R, Alzubaidi M, Ghayyib S. "Fatty liver disease in children and adolescents with type 1 diabetes mellitus (clinical and diagnostic aspects)". J Clin Gastroenterol Hepatol. 2018; 2(2): 14. DOI: 10.21767/2575-7733.1000043.

[10] Khandelwal R, Dassanayake AS, Conjeevaram HS, Singh SP. "Non-alcoholic fatty liver disease in diabetes: When to refer to the hepatologist?". World J. Diabetes. 2021; 12(9): 1479. DOI: 10.4239/wjd.v12.i9.1479.

[11] King KM, Jaggers JR, Della LJ, McKay T, Watson S, Kozerski AE, et al. "Association between physical activity and sport participation on hemoglobin A1c among children and adolescents with type 1 diabetes". Int J Environ Res Public Health. 2021; 18(14): 7490. DOI: 10.3390/metabo12111017.

[12] Grabia M, Markiewicz-Żukowska R, Socha K, Polkowska A, Zasim A, Boruch K, et al. "Prevalence of metabolic syndrome in relation to cardiovascular biomarkers and dietary factors among adolescents with type 1 diabetes mellitus". Nutr. 2022; 14(12). DOI: 10.3390/nu14122435.

[13] de Gonzalo-Calvo D, Dávalos A, Montero A, García-González Á, Tyshkovska I, González-Medina A, et al. "Circulating inflammatory miRNA signature in response to different doses of aerobic exercise". J. Appl. Physiol. 2015; 119(2): 124-34. DOI: 10.1152/japplphysiol.00077.2015.

[14] Fernández-Sanjurjo M, de Gonzalo-Calvo D, Fernández-García B, Díez-Robles S, Martínez-Canal Á, Olmedillas H, et al. "Circulating microRNA as emerging biomarkers of exercise". Exerc Sport Sci Rev. 2018; 46(3): 160-71. DOI: 10.1249/JES.0000000000000148.

[15] Femminò S, Pagliaro P. "Exercise prevents cardiovascular dysfunctions in diabetes through miRNAs modulation". Non-coding RNA Investig. 2021; 5: 1. DOI: 10.21037/ncri-20-8.

[16] Grieco GE, Dotta F. The Essential Role of MicroRNAs in Diabetes Mellitus: Regulators of β Cell Function And Potential Disease Biomarkers. Ph.D thesis. 2020.

[17] Friedrich M, Pracht K, Mashreghi MF, Jäck HM, Radbruch A, Seliger B. "The role of the miR‐148/‐152 family in physiology and disease". Eur. J. Immunol. 2017; 47(12): 2026-38. DOI: 10.1002/eji.201747132.

[18] Improta Caria AC, Nonaka CKV, Pereira CS, Soares MBP, Macambira SG, Souza BSdF. "Exercise training-induced changes in microRNAs: beneficial regulatory effects in hypertension, type 2 diabetes, and obesity". Int. J. Mol. Sci. 2018; 19(11): 3608. DOI: 10.3390/ijms19113608.

[19] Liu S, Wu W, Tang F, Shen M, Xu W, Zhao S. "MicroRNA-21: A critical pathogenic factor of diabetic nephropathy". Front. Endocrinol. 2022: 1330. DOI: 10.3389/fendo.2022.895010.

[20] Margaritis K, Margioula-Siarkou G, Giza S, Kotanidou EP, Tsinopoulou VR, Christoforidis A, et al. "Micro-RNA implications in type-1 diabetes mellitus: A review of literature". Int. J. Mol. Sci. 2021; 22(22): 12165. DOI: 10.3390/ijms222212165.

[21] Shi C, Zhang M, Tong M, Yang L, Pang L, Chen L, et al. "miR-148a is associated with obesity and modulates adipocyte differentiation of mesenchymal stem cells through Wnt signaling". Sci. Rep. 2015; 5(1): 9930. DOI: 10.1038/srep09930.

[22] Nascimento LRd, Domingueti CP. "MicroRNAs: new biomarkers and promising therapeutic targets for diabetic kidney disease". Braz. J. Nephrol. 2019; 41: 412-22. DOI: 10.1590/2175-8239-JBN-2018-0165.

[23] Matsuzaka A, Takahashi Y, Yamazoe M, Kumakura N, Ikeda A, Wilk B, et al. "Validity of the multistage 20-m shuttle-run test for Japanese children, adolescents, and adults". Pediatr. Exerc. Sci. 2004; 16(2): 113-25. DOI: 10.1123/pes.16.2.113.

[25] Tan Y, Lu X, Cheng Z, Pan G, Liu S, Apiziaji P, et al. "miR-148a regulates the stem cell-like side populations distribution by affecting the expression of ACVR1 in esophageal squamous cell carcinoma". Onco Targets Ther. 2020: 8079-94. DOI: 10.2147/OTT.S248925.

[26] Yuan K, Lian Z, Sun B, Clayton MM, Ng IO, Feitelson MA. "Role of miR-148a in hepatitis B associated hepatocellular carcinoma". PloS one. 2012; 7(4): e35331. DOI: 10.1371/journal.pone.0035331.

[27] Chen J, Bai X, Wu Q, Chen L, Wang H, Zhang J. "Exercise protects against cognitive injury and inflammation in alzheimer’s disease through elevating miR-148a-3p. Neurosci. 2023; 513: 126-33. DOI: 10.1016/j.neuroscience.2023.01.008.

[28] Li Y, Deng X, Zeng X, Peng X. "The role of Mir-148a in cancer". J. Cancer. 2016; 7(10): 1233. DOI: 10.7150/jca.14616.

[29] Nielsen S, Åkerström T, Rinnov A, Yfanti C, Scheele C, Pedersen BK, et al. "The miRNA plasma signature in response to acute aerobic exercise and endurance training". PloS one. 2014; 9(2): e87308. DOI: 10.1371/journal.pone.0087308.

[30] Vasu S, Kumano K, Darden CM, Rahman I, Lawrence MC, Naziruddin B. "MicroRNA signatures as future biomarkers for diagnosis of diabetes states". Cell. 2019; 8(12): 1533. DOI: 10.3390/cells8121533.

[31] Jin X, Hao Z, Zhao M, Shen J, Ke N, Song Y, et al. "MicroRNA-148a regulates the proliferation and differentiation of ovine preadipocytes by targeting PTEN". Animals (Basel). 2021; 11(3): 820. DOI: 10.3390/ani11030820.

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Volume 17, Issue 1January 2025Pages 43-54

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Volume 17, Issue 1
January 2025
Pages 43-54